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Introduction

‘…as the dredge cleared the surface, we saw it full andoverflowing with every form of sea life it is possible to imagine…most conspicuous of all were the giant sea-spiders, red in color,

and from 6 to 7 inches across the legs.’

From South with Mawson by C. F. Laserson, zoologist on the1911–1914 Australasian Expedition (Laserson, 1947).

For well over a century, zoologists and explorers to the poles haveobserved that organisms there can reach remarkably large sizes.Early explorers from the Antarctic, such as Laserson from theAustralasian expedition, wrote in their populist travel journalsabout the giant animals obtained from nearshore marine dredging(Laserson, 1947); the organisms collected by these expeditionswere written up in scientific journals of the day (e.g. Eights, 1856;Hodgson, 1905; Dall, 1907). Sea spiders the size of dinner plates,and other bizarre life discovered by these explorers, added to themystery and excitement surrounding the Antarctic continent andhelped to fuel the Heroic Age of Antarctic Exploration.

From a biologist’s perspective, polar gigantism fascinatesbecause it is bizarre, and because gigantism is a potentiallypowerful tool for understanding the physical, ecological andevolutionary principles that govern the evolution of body size.Body size is a key determinant of how organisms interact with theirenvironments (Hildrew et al., 2007), and understanding theevolution of body size has been a central focus of evolutionary

biology (Roff, 1992; Stearns, 1992; Blanckenhorn, 2000). Thatpolar giants occur in many distantly related taxa indicates thatgigantism has evolved independently many times, suggesting thatsome master mechanism drives the pattern (Chapelle and Peck,1999). This has in turn led to questions about patterns of absence,i.e. why some polar groups contain no giants. By ‘going toextremes’, biologists hope to understand factors that driveevolution in the ecosphere in general.

Though gigantism has also been reported from terrestrialorganisms [e.g. lichens (Øvstedal and Smith, 2001)], we focus onorganisms from the marine environment because the terrestrialAntarctic fauna is comparatively sparse, whereas the polar oceansare home to a fauna that is rich and often strange. In terms ofmultiple metrics, conditions in polar oceans are extreme. Polaroceans are the coldest large bodies of water on earth, withtemperatures at the freezing point of seawater (–1.8°C) duringwinter in the Arctic and year-round near the continental coast andice shelves of the Southern Ocean (Clarke, 2003). Polar ectotherms,which do not produce substantial metabolic heat, move, grow, feedand reproduce at body temperatures so cold that temperate andtropical relatives would be torpid or even frozen solid. Numerousmetabolic, biochemical, life history and physiological adaptationshave been described that help polar ectotherms to function at thesetemperatures (e.g. DeVries, 1988; Clarke, 1991; Clarke, 1998).

Polar environments have other unique characteristics. Abovethe Arctic and Antarctic circles, day length cycles annuallybetween 0 and 24h, driving dramatic annual cycles ofproductivity and, therefore, food availability for filter and

SummaryBeginning with the earliest expeditions to the poles, over 100years ago, scientists have compiled an impressive list of polar taxawhose body sizes are unusually large. This phenomenon has become known as ʻpolar gigantismʼ. In the intervening years,biologists have proposed a multitude of hypotheses to explain polar gigantism. These hypotheses run the gamut from invokingrelease from physical and physiological constraints, to systematic changes in developmental trajectories, to community-leveloutcomes of broader ecological and evolutionary processes. Here we review polar gigantism and emphasize two main problems.The first is to determine the true strength and generality of this pattern: how prevalent is polar gigantism across taxonomic units?Despite many published descriptions of polar giants, we still have a poor grasp of whether these species are unusual outliers orrepresent more systematic shifts in distributions of body size. Indeed, current data indicate that some groups show gigantism atthe poles whereas others show nanism. The second problem is to identify underlying mechanisms or processes that could drivetaxa, or even just allow them, to evolve especially large body size. The contenders are diverse and no clear winner has yetemerged. Distinguishing among the contenders will require better sampling of taxa in both temperate and polar waters andsustained efforts by comparative physiologists and evolutionary ecologists in a strongly comparative framework.

Key words: body size, evolution, Bergmann, carbonate, temperature–size rule, temperature, oxygen, polar ocean, Arctic, Antarctic, optimalitymodels, life history.

Received 11 November 2011; Accepted 21 February 2012

The Journal of Experimental Biology 215, 1995-2002© 2012. Published by The Company of Biologists Ltddoi:10.1242/jeb.067066

COMMENTARY

Why might they be giants? Towards an understanding of polar gigantism

Amy L. Moran1,* and H. Arthur Woods2

1Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA and 2Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA

*Author for correspondence (moran@clemson.edu)

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suspension feeders (Clarke, 2003). This cycle of feast and faminehas been linked to unusually slow growth rates, enhancedresistance to starvation, and reduced ecological competition(Lindstedt and Boyce, 1985; Cushman et al., 1993; Arnett andGotelli, 2003). Seawater in the Southern Ocean is also rich in O2

and silica (Ragueneau et al., 2000), and building shells and othercalcium carbonate structures is both more difficult and moreenergetically expensive in the cold (McClintock et al., 2009).Organisms in the Antarctic have evolved in relative isolationunder these conditions for millions of years, making theAntarctic a ‘natural laboratory for tackling fundamentalquestions’ (Clarke, 2003). Below, we explore the links betweenthe physical, chemical and biological environments of polar seasand the evolution of gigantism.

Who are the giants?Polar gigantism has been reported among many taxa of marineorganisms, including copepods (Hop et al., 2006), pteropodmolluscs (Weslawski et al., 2009), cephalopod molluscs (Rosa andSiebel, 2010), ctenophores (Barnes, 2005) (Fig.1), chaetognaths(MacLaren, 1966), foraminiferans (Mikhalevich, 2004), amphipodcrustaceans (DeBroyer, 1977), isopod crustaceans (Menzies andGeorge, 1968; Luxmoore, 1982), sponges (Fig.2) (Dayton andRobillard, 1971), polychaete annelids (Hartman, 1964),echinoderms (Dahm, 1996) and pycnogonids (sea spiders; Fig.3)(Child, 1995). Polar gigantism has also been reported from thefossil record [trilobites (Gutiérrez-Marco et al., 2009)]. We firstdiscuss definitions of ‘gigantism’ and explore how common thisphenomenon is in polar systems.

Clearly gigantism is relative, requiring comparison with otherrelated taxa. In early studies of isopod and tanaid crustaceans,Wolff (Wolff, 1956a; Wolff, 1956b) noted that the largest specieswithin genera occurred in the Antarctic and the deep sea. Arnaud(Arnaud, 1974), in what is still the most extensive review of polargigantism, reported the lengths of the largest polar organisms whileacknowledging that size must be considered in the context of eachphylogenetic group. Other polar researchers have applied morequantitative criteria; DeBroyer (DeBroyer, 1977) categorized aspecies as giant if it was at least twice as large as the mean bodysize in its genus, and Chapelle and Peck (Chapelle and Peck, 1999)

if its body length was in the top 5% for its taxon within a particularhabitat.

Although there is no universal definition of polar gigantism,comparative evidence that it exists is strong, at least in sometaxonomic groups. Perhaps the clearest example comes fromamphipods in the suborder Gammaridae, shrimplike crustaceansthat are diverse and that contain close relatives living in both polarand non-polar regions (DeBroyer, 1977; Gomes et al., 1993).DeBroyer (DeBroyer, 1977) analyzed gammarid body sizes andfound strong evidence for large body size at the poles, particularlyin the Antarctic; 31% of species in the Southern Ocean had bodylengths >2� larger than the mean body size of their genus,compared with 28% in the Arctic, 21% in the deep sea and 0.8%in the tropics. Thus, although giants occur in most habitats, theyare more common at the poles. In isopods of the cosmopolitangenus Serolis, maximum body size increased with latitude and nosmall-bodied species occurred in the Southern Ocean (Fig.4)(Luxmoore, 1982).

Although the literature contains many other references togigantism, few examples have been analyzed in a comparativecontext. Gigantism among pycnogonids is frequently cited (e.g.Dell, 1972; Arnaud, 1974; Child, 1995; Clarke and Johnston, 2003)and would be a good subject for additional comparative workbecause sea spiders are found worldwide, yet are abundant anddiverse in the Southern Ocean (Child, 1995; Munilla and Soler-Membrives, 2009). The largest pycnogonids occur in the polaroceans and the deep sea (Arnaud and Bamber, 1988). Glass sponges(Class Hexactinellida) provide another spectacular example (Dell,1972): the barrel sponge Anoxycalyx (Scolymastra) jouboni canreach 2m in height and 1.5m in diameter (Dayton and Robillard,1971). The ribbon worm Parbolasia corrugatus can reach 2m inlength and 100g in body mass (Davison and Franklin, 2002),making it among the world’s largest nemerteans by mass (Arnaud,1974), and at least 14 species of polychaete worms (phylumAnnelida) from the Antarctic have body lengths >10cm (Hartmann,1964), including Ophioglycera eximia, which reaches 76cm.However, although these examples are spectacular, demonstratinggigantism via the comparative method has been impossible in manycases because of low taxon sampling and a lack of detailedphylogenies.

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Fig.1. Diver A. L. Moran behind a large beroid ctenophore, near McMurdoStation, Antarctica. Photo by B. Miller.

Fig.2. Diver S. Rupp pictured near McMurdo Station, Antarctica, amongstspecimens of the glass sponge Anoxycalyx jouboni. Photo by R. Robbins.

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Many other major groups lack giants or even trend towards high-latitude nanism (unusually small body size). In the bivalve molluscs(clams, scallops and oysters), Nicol (Nicol, 1967) found no high-latitude species, towards either pole, that he considered large. Infact, many are unusually small [<10mm in length (Nicol, 1967)].Prosobranch gastropod molluscs (shelled snails) also lack giants atthe poles, and tend to be small in the Antarctic (but not the Arctic)(Arnaud, 1974). Other groups that lack giants, or that tend towardspolar dwarfism, include scaphopod molluscs (tusk shells) (Arnaud,1974), chitons (class Polyplacophora) (Arnaud, 1974), fish(Andriashev, 1965; Knox, 2007) and brachiopods (Arnaud, 1974;Peck and Harper, 2010). Moreover, even higher taxa that containpolar giants may have subgroups that do not. For example, in theamphipod family Lyssianasidae – which is in the suborderGammaridae, discussed above as containing giants – polar speciesare not unusually large compared with cold-temperate species.High-latitude species tend to be larger than average, but this trendis driven by a lack of large-bodied species in the tropics rather thanthe presence of giants at the poles (Steele, 1983).

This diversity of examples demonstrates that studying polargigantism is a two-part problem. The first is to determine whetherpolar gigantism is systematic or represents excessive attention paidto a few unusual taxa. In part, this issue stems from a historicpaucity of studies on polar taxa, and of taxonomic specialistsworking on Antarctic groups (Arnaud, 1974). Likewise, polarwaters have historically been poorly sampled, particularly deeperzones (Griffiths et al., 2009); however, substantial internationalefforts have recently been made to further explore and describe thebiological diversity of the Southern Ocean [e.g. the Census ofAntarctic Marine Life, part of the International Polar Year researcheffort; described in Griffiths et al. (Griffiths et al., 2011)]. Newfocus on the diversity and relatedness of polar organisms, combinedwith modern systematic and comparative methods, will providenew tools for detecting gigantism, or the lack thereof.

The second part of the problem is to determine, for taxa thatshow polar gigantism, whether some common factor drives, orallows, evolution of large body size or, instead, whether manyfactors contribute idiosyncratically in different taxa. The rest of our

review focuses on this second problem. Many hypotheses havebeen suggested to explain polar gigantism, and these provide a largeset of alternative but non-exclusive potential mechanisms.

Why might they be giants?Like other biogeographic patterns, polar gigantism likely will defysimple explanatory frameworks. One set of theories invokesbiophysical and physiological explanations; these focus on the effectsof unusual levels of environmental factors in polar environments,particularly temperature, oxygen and carbonate chemistry. A secondset of ideas invokes biogeographic and ecological explanations,which draw historical links between polar oceans and other regionsthat share taxa, or which invoke unusual ecological conditions at thepoles. A third set focuses on developmental plasticity and evolution.These explanations tend to analyze life history trade-offs betweengrowth, fecundity and mortality associated with latitudinal changesin competition and predation, temperature and resource availability.Not all possible mechanisms are mutually exclusive. We agree withAngilletta et al. (Angilletta et al., 2004) that any broad theory of bodysize will have to be multivariate, in the sense that multiple factorsprobably contribute to gigantism in taxon-dependent ways. Thisprognosis could be viewed as gloomy, but it likely reflects the messy,historical, contingent nature of biology better than any simpleralternative.

Below we organize the discussion around the three levels ofanalysis outlined above, with caveats. The first is that several of theideas (e.g. the temperature–size rule) do not fit readily into ourorganizational scheme because they integrate elements from acrosslevels of biological organization; for convenience, we discuss thetemperature–size rule in the section on developmental plasticity andevolution. Second, most of the ideas focus on temperature. Atemperature-centered approach is appropriate: cold, stabletemperatures are a dominant characteristic of polar marine habitats,temperature has pervasive effects on all biological processes, andmost studies to date have focused on temperature as a causal agent.Nevertheless, it is not certain that low temperature has driven polargigantism either alone or in interaction with other factors. Therefore,third, we also consider a smaller set of non-temperature hypotheses.

Fig.3. Giant Antarctic sea spider (phylum Pycnogonidae), probablyColossendeis megalonyx, photographed near McMurdo Station, Antarctica.The gloved finger of a diver is visible at the bottom left. Photo by B. Miller.

Minimum latitude (°S)0 10 20 30 40 50 60 70

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Fig.4. Variation in size with latitude of isopod crustaceans in the genusSerolis. Maximum length of adult males of the 41 species that occur at depthsof <200m plotted against their minimum recorded latitude. Spearmanʼs rankcorrelation coefficient, r20.650 (P<0.001). [Redrawn and reprinted from J.Exp. Mar. Biol. Ecol. 56, Luxmoore, R. A., Moulting and growth in serolidisopods, p. 82. Copyright (1982), with permission from Elsevier.]

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Biophysical and physiological explanationsOxygen hypothesis

The oxygen hypothesis, proposed by Chapelle and Peck (Chapelleand Peck, 1999), states that polar gigantism stems from highoxygen availability coupled with low metabolic rates. The authorssurveyed maximum body sizes in collections of amphipodcrustaceans from different habitats, finding that the size of‘giants’ in each locality – defined as the largest 5% of species ineach habitat – correlated strongly with potential oxygenavailability determined from water temperature (Fig.5). Theyconcluded that ‘maximum potential size is limited by oxygenavailability’. The oxygen hypothesis has received considerableattention (see McClain and Rex, 2001; Chapelle and Peck, 2004;Woods and Moran, 2008; Woods et al., 2009; McClain and Boyer,2009; Klok et al., 2009; Verberk and Bilton, 2011; Verberk et al.,2011) and also considerable support in some taxa, particularlyamphipods (e.g. Chapelle and Peck, 2004). Moreover, there is asubstantial subset of literature suggesting that atmospheric O2 andorganismal body size have been linked through history (for areview, see Payne et al., 2011). However, even among thegammarid amphipods, which are poster children for polargigantism, many polar representatives are tiny, and only a smallfraction of taxa reach very large sizes even in regions of thehighest oxygen availability (Chapelle, 2001; Chapelle and Peck,2004). Thus, the main effect of the high ratio of oxygenavailability to demand at cold temperatures is to increase thewindow of body sizes into which lineages diversify, rather thanto drive the evolution of large body sizes. Other factors must beinvoked to explain selection for large body size.

One appeal of the oxygen hypothesis is that it is experimentallytractable, in that it can be directly tested by assessing whether large-bodied organisms perform worse in hypoxia than small-bodiedones. Such a prediction follows naturally from the oxygenhypothesis, which implies that large-bodied organisms are closer tosome upper limit in body size beyond which oxygen supplies wouldbecome inadequate. In one experimental test, Peck et al. (Peck etal., 2007) found that larger-bodied Antarctic clams had reducedburying performance in hypoxia compared with smaller

conspecifics. By contrast, Woods et al. (Woods et al., 2009) useda righting assay to assess whether large-bodied Antarcticpycnogonids performed worse in hypoxia than small-bodiedpycnogonids. In this case, the data said otherwise: regardless ofbody size, all pycnogonids performed worse in hypoxia, and therewas no hint of size dependence in the effects.

The straightforward interpretation of the data of Woods et al.(Woods et al., 2009) is that they reject the oxygen hypothesis.However, a more nuanced interpretation is possible. In particular,although cold temperatures and plentiful oxygen may have allowedthe repeated evolution of gigantic Antarctic pycnogonids, there hasbeen superimposed on those events a process of coadaptation bydifferent, linked components of the respiratory system, and trade-offs among multiple costs and benefits of having cuticles of someparticular permeability. Pycnogonids obtain oxygen via diffusiondirectly across the chitinous exoskeleton, and diffusion is facilitatedthrough pits and channels that make up >30% of the cuticularsurface (Davenport et al., 1987). The lack of any size-dependenteffects of hypoxia on performance might be explained by selectionacting to reduce the ‘excess’ oxygen diffusion capacity of smallpolar pycnogonids, perhaps to increase resistance to predators orbuckling forces, or to protect them from excessively high levels ofinternal oxygen, which could produce damaging reactive oxygenspecies. Conversely, in the evolutionary trajectory from small tolarge body sizes, perhaps giant pycnogonids obtain adequateoxygen, even when working hard, through cuticles that haveevolved to be especially permeable to oxygen. These outcomescould be interpreted as reflecting either symmorphosis (the idea thatorganismal form and function are closely matched across levels ofbiological organization) or size-dependent shifts in the relativevalue of the costs and benefits of having a particular cuticularpermeability.

The links between body size, environmental oxygen availabilityand performance have been used to argue that as marine and aquaticenvironments warm, small body size will be favored and giants willbe among the first to disappear (Chapelle and Peck, 2004;Daufresne et al., 2009; Pörtner, 2010). Our arguments above,however, imply that temperature-dependent physiological systems(that is, essentially all systems) are more co-adapted to each otherthan they are to the size of the organism. Thus, there is no simpleprediction possible about the relationship between size andvulnerability, at least with respect to individual organisms (ratherthan evolving lineages) and physical aspects of the environmentsuch as temperature or oxygen availability.

Carbonate and silica chemistry in Antarctic watersPolar seas, in particular the Southern Ocean, have unusualcarbonate and silica chemistry, possibly affecting which taxa attaingiant sizes. Some marine taxa use silica in their skeletons, includingboth the single-celled diatoms and radiolarians and the multicellular‘glass’ sponges (phylum Porifera, class Hexactinellidae). Silica isoften limiting in tropical and subtropical waters, but is moreabundant in the Southern Ocean because of upwelling of silica-richdeep water (Ragueneau et al., 2000). Plentiful silica may contributeto the large size of silica-based organisms such as the giantAntarctic glass barrel sponge, Anoxycalyx (Scolymastra) jouboni(Arnaud, 1974). However, the availability of silica does not lead togigantism in all silicaceous organisms; though the shells ofAntarctic radiolarians are more heavily silicified than the shells ofwarm-water relatives, their cell sizes are no larger (Lazarus et al.,2009).

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Fig.5. The relationship between water oxygen content (at 100% saturation)and body size of the largest 5% of species of amphipod crustaceans in agiven habitat (TS95/5). Orange circles are marine sites; blue circles arereduced-salinity sites. Reprinted with permission from MacmillianPublishers Ltd: Nature, Chapelle, G., and Peck, L. S., Polar gigantismdictated by oxygen availability, pp. 114-115, Fig.2b, 1999.

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Why don’t some other groups of organisms attain giant sizes atthe poles? The answer may also be determined by ocean chemistry,particularly levels of calcium carbonate (CaCO3). The solubility ofCO2 increases with decreasing temperature, and, by taking up moreCO2, cold waters become relatively more acidified. In turn, coldwater and acidification enhance the dissolution of CaCO3,potentially making calcification difficult and costly at coldtemperatures (reviewed in Doney et al., 2009). This problem ismost acute in the Southern Ocean, where temperatures are <0°Cyear-round, dissolved CO2 is high and there is little input ofcarbonate from freshwater runoff. In this corrosive environment,animals with skeletons based on CaCO3, such as echinoderms,shelled molluscs and stony corals, may be limited to small sizes bythe high metabolic expense of building and maintaining theirskeletons (Arnaud, 1974). Some groups, such as the shelledmolluscs, indeed lack polar giants, and Antarctic animals withcalcareous skeletons are often thin and fragile compared with theirtemperate relatives. However, other calcifying groups such as theechinoderms have large Antarctic representatives [e.g. the starfishMegapteraster (Arnaud, 1974)]. An alternative explanation forfragile calcareous exoskeletons is the lack of durophagous(crushing) predators in the Southern Ocean (Aronson et al., 2009).

Biogeographic and ecological explanationsMonsters from the deep

Many authors have noted that taxa from the polar oceans,particularly the Southern Ocean, share common evolutionaryhistories with taxa from the deep sea (Zinsmeister and Feldmann,1984; Clarke, 2003). ‘Abyssal gigantism’ occurs in some of thegroups also noted for polar gigantism, including pycnogonids,isopods, and amphipods. Does polar gigantism reflect invasion ofthe Southern Ocean by large-bodied animals from the deep sea?Perhaps, but the evolutionary history of the benthic Southern Oceanfauna is complex, likely with movement in both directions (shelfto deep and vice versa) (Brandt et al., 2007a; Strugnell et al., 2011).As data from the recent ANDEEP program, which samples thedeep-water fauna of the Southern Ocean, are analyzed (e.g. Brandtet al., 2007b), such links, if present, should become apparent.

We suggest that the explanation that polar giants are ‘monstersfrom the deep’ is less than satisfying, because although it providesa proximate evolutionary explanation, it also pushes off themechanistic explanation into other biomes: why then do large-bodied individuals evolve in abyssal zones? Abyssal waters sharesome features of polar waters, such as cold and stable temperatures,but other evolutionary forces that shape body size in the two regionslikely differ and lead to contrasting outcomes in the two habitats;e.g. although gigantism is common among deep-sea shelledgastropods (McClain and Rex, 2001), it is not in polar regions(Arnaud, 1974).

Starvation resistance and the seasonal availability of resourcesIn polar seas, primary production fluctuates circannually, from highin the summer to virtually zero in the winter. Compared with smallanimals, large animals may resist starvation better (Cushman et al.,1993; Arnett and Gotelli, 2003), which may drive the evolution oflarge size in environments that impose intermittent starvation(Ashton, 2002; Blackburn et al., 1999). Strong seasonality may alsolimit the total number of species that an environment can support,which may alleviate interspecific competition, at least duringperiods when resources are available (Geist, 1987; Blackburn et al.,1999; Zeveloff and Boyce, 1988). Among polar ectotherms,however, metabolic rates are extremely low (Clarke, 1983) and

even very small animals can live for months without feeding(Shilling and Manahan, 1994). Likewise, organisms that are mostlikely to be affected by low productivity in winter are filter feedersthat rely on phytoplankton. In at least some groups of filter feeders,however, such as bivalves, polar gigantism has not been observed;in fact, this group tends towards nanism (Arnaud, 1974). Thus,resource availability does not provide an overarching frameworkfor polar gigantism.

Latitudinal changes in resource qualityThe quality of food resources for herbivores may increase withlatitude (e.g. Bolser and Hay, 1996), and this may be related tolatitudinal patterns of body size (for a review, see Ho et al., 2010).This hypothesis was tested by Ho et al. (Ho et al., 2010), who foundthat herbivorous ectotherms from a range of habitats (marine,terrestrial) in the Northern Hemisphere grew to larger sizes whenreared on high-latitude diets. We know of no direct tests of this ideawith polar organisms. In general, Antarctic macroalgae (which arethe food of many herbivores in regions where ice cover does notpreclude macroalgal growth) have stronger chemical defenses thando Arctic algae (Amsler et al., 2005), suggesting that this hypothesisis more relevant to northern than to southern polar gigantism.

Interspecific interactionsThe Southern Ocean has a particularly unusual faunal composition.This region saw the onset of oceanic cooling and glaciation thatlikely scoured the continental shelves periodically beginning in theearly Miocene, reducing regional diversity and eliminating somegroups that are common elsewhere in the Southern Hemisphere(Anderson, 1999; Brandt, 2005). In particular, durophagouspredators – such as sharks, skates and decapod crustaceans thatbreak hard-shelled prey – have been absent from the SouthernOcean since the Eocene (Aronson et al., 2009). In their place, themost important predators now are asteroids, nemertean worms,isopods, amphipods, crustaceans and pycnogonids (Aronson et al.,2009), and this shift may have selected some lineages for largerbody size (Barnes and Arnold, 2001).

The island rule of biogeography (Foster, 1964; Case, 1978)provides a framework for understanding the ecological factorsdriving the evolution of body size when animals invade novel,isolated habitats. When species invade islands, small mammalsoften evolve larger sizes whereas large-bodied taxa tend to shrink(Foster, 1964; reviewed in Millien and Damuth, 2004). The islandrule cannot be explained by oxygen or temperature, because theserarely differ between islands and nearby mainlands. Rather, islandgigantism is generally attributed to an escape from mainlandpredators and competitors, whereas nanism has been ascribed toreduced resource availability on islands (Foster, 1964). TheSouthern Ocean has many island-like characteristics: it isphysically isolated and physiologically distinct, and many taxahave undergone ecological release from historical predators andcompetitors. We suggest that such factors, coupled with the raisingof the ceiling on possible body sizes by the high ratio of oxygensupply to demand, may have led to the evolution of giants in manytaxa. However, as on islands, most Antarctic taxa are neither giantsnor dwarfs (Case, 1974).

Developmental and evolutionary explanationsLatitudinal gradients in body size and the temperature–size rule

Any temperature-related explanation must articulate therelationship between polar gigantism and two better-knownpatterns: latitudinal gradients in body size and the temperature–size

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rule. Latitudinal gradients in body size represent a generalizationof Bergmann’s rule, which states that, within genera of endothermicvertebrates, species at higher latitudes tend to have larger bodysizes (Bergmann, 1847; Watt et al., 2010). Bergmann proposed thatlarger individuals, with smaller surface-area-to-volume ratios,could more easily maintain high, stable body temperatures in coldenvironments. In general, ectotherms do not face similarthermoregulatory problems. However, many ectothermic taxanevertheless show similar latitudinal gradients in body size(Angilletta and Dunham, 2003; Walters and Hassall, 2006;Pincheira-Donoso et al., 2008; Wilson, 2009; Lee and Boulding,2010). Because Bergmann’s rule applies specifically toendothermic vertebrates (Watt et al., 2010), we refer to the broaderpattern, which includes ectotherms, as ‘the latitude–size rule’.

Clearly, polar gigantism could be a high-latitude endpoint of thelatitude–size rule applied to marine species; therefore, generalexplanations for this pattern may, in the end, also explain polargigantism. Despite a broad search for explanatory mechanisms, noconsensus has emerged. The four primary contenders, whichpartially overlap hypotheses outlined above, are that latitude–sizeclines reflect: (1) artifacts of phylogenetic history, because at highlatitudes, large-bodied lineages are more likely to establish anddiversify; (2) size-dependent variation between species in rates ofmigration or ability to establish in new areas; (3) variation inresistance to starvation (see above); and (4) variation in ability ofspecies to conserve or dissipate heat (Cushman et al., 1993; Gastonand Blackburn, 2000). The latter mechanism, although plausible forterrestrial ectotherms (in air), is unlikely to be important for mostmarine ectotherms, which are essentially always in thermalequilibrium with their surroundings.

Polar gigantism and the latitude–size rule are both related to thetemperature–size rule proposed by Atkinson (Atkinson, 1994;Atkinson, 1996), which focuses on developmental plasticity inresponse to rearing temperature. It is now evident that ectothermsgrowing in colder temperatures tend to reach larger final body sizesthan do conspecifics in warmer temperatures (see Atkinson andSibly, 1996; Atkinson et al., 2006; and references therein). In abroad review, Atkinson (Atkinson, 1994) found that in >80% ofspecies, organisms grew larger when reared in cooler temperatures,in some cases by large margins. A string of papers in the past20years has sought to explain this pattern in satisfactory theoreticalterms. Most of the models hinge on the idea that rate processesinvolved in growth or differentiation, or that the rates of growth,predation and fecundity, are differentially sensitive to temperature(reviewed by Angilletta et al., 2004; see also Perrin, 1995;Angilletta, 2009; Arendt, 2011). However, there is a more generalreason to suspect that the temperature–size rule cannot not explainpolar gigantism fully: the magnitude of the temperature–size rulewithin species does not appear, in general, to be large enough toaccount for the observed evolutionary differences in body sizeamong species, with the caveat that there are few data available forevaluating this claim quantitatively.

Cold-driven selection for large offspring sizeAnother, less obvious form of gigantism common in polar waters isfound in eggs, embryos and larvae. Thorson (Thorson, 1950) andRass (Rass, 1935) first identified this biogeographic trend, in whichmarine invertebrates and fish at high latitudes produce fewer, largeroffspring than their relatives elsewhere. ‘Thorson’s rule’(Mileikovsky, 1971), as it is now called, ascribes this pattern toevolutionary shifts from planktotrophy (having larvae that requireexogenous food to complete development) to lecithotrophy (larvae

that can complete development without exogenous particulate food);lecithotrophy may be advantageous in polar climates because of longdevelopmental times coupled with extreme seasonality in foodavailability (Thorson, 1950; Laptikhovsky, 2006). Even amongplanktotrophs, however, egg size tends to be large in polar regions(Thorson, 1950; Marshall, 1953). Rass (Rass, 1935) andLaptikhovsky (Laptikhovsky, 2006) point out that cold temperaturesinduce fish and invertebrates to produce larger eggs (plasticity); thisis one oft-cited component of the temperature–size rule. Large eggsize may also reflect selection for increased maternal provisioning tooffset: (1) a poor or seasonally brief feeding environment (Thorson,1950; Marshall, 1953), (2) greater competition in polar environments(Alekseev, 1981), or (3) the prolonged development that occurs atcold temperatures (Marshall, 1953).

Polar ‘embryo gigantism’ appears to be considerably morewidespread than adult gigantism; for example, although the eggsand larvae of Antarctic fish are large in general (Marshall, 1953;and others reviewed in Knox, 2007), to our knowledge the adultsof Antarctic fish are not considered large (see Marshall, 1953;Johnston et al., 2003). Among polar nudibranchs, eggs and embryoscan be dramatically larger than those of temperate relatives (Woodsand Moran, 2008), but sizes of adults are only modestly so.Comprehensive comparative studies are still lacking, but thispattern suggests that selection, plasticity or their combination actstrongly on oogenesis to increase the size of eggs, larvae andjuveniles in polar environments. Polar gigantism among embryosprovides a rich but unmined context for testing theories of optimaloffspring size (e.g. Smith and Fretwell, 1974; Yampolsky andScheiner, 1996; Fox and Czesak, 2000). Note that this pattern(relatively larger embryos compared with adults) runs counter tothe developmental effects of temperature across stages: Forster etal. (Forster et al., 2011) showed that developmental temperaturegenerally had greater effects on adult size than on offspring size.This mismatch further undermines the possibility that thetemperature–size rule accounts generally for polar gigantism (seepreceding section).

ConclusionsThe extreme, constant cold of polar marine environments has beenimplicated in many unusual traits, including gigantism, extremestenothermality, freeze tolerance and changes in oxygen carryingand storage capacity. In general, these traits are interpreted asadaptive, though we do not always understand the underlyingfactors that have driven their evolution, or whether some may be‘disaptations’ allowed by polar conditions (Sidell and O’Brien,2006). Of polar phenomena, gigantism may be the most complexto unravel because body size is so central to ecological andevolutionary processes.

Our review has broken the problem of polar gigantism into twomajor issues. The first is, surprisingly, to determine even howcommon polar gigantism is. Although there are many convincingreports of polar giants, it remains unclear whether these examplesreflect a few attention-grabbing outliers or more pervasive shifts indistributions of body size. Resolving this issue will requiresystematic sampling of species and body sizes in phylogeneticcontexts. The second problem is to link patterns of body size toexplanatory mechanisms. We distinguish at least eight majorhypotheses above; each deserves additional theoretical andexperimental work. Finally, looming above the set of individualhypotheses is the meta-problem of whether just one hypothesis willemerge as dominant or, alternatively, whether multiple hypothesescontribute to the pattern in taxon- and context-dependent ways. The

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way forward, we think, is to view these possibilities asopportunities: understanding the factors underlying polar gigantismwill both shed light on the fundamental processes underlying bodysize evolution and provide insight into the challenges that polarorganisms will face during future climate change.

AcknowledgementsWe thank B. Miller and R. Robbins for permission to use their photographs ofAntarctic invertebrates that display gigantism. We also thank P. Kitaeff, B. Miller,L. Mullen, C. Shields, J. Sprague and the staff of McMurdo Station, Antarctica, forresearch assistance and support related to this work. Finally, we thank P. Conveyand an anonymous reviewer for comments on an earlier draft that substantiallyclarified the manuscript.

FundingThis work was supported by the United States National Science Foundation [ANT-0551969 to A.L.M. and ANT-0440577 to H.A.W.], and by Clemson University andthe University of Montana.

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